Analysis of Ribosomal Protein Gene Structures: Implications for Intron Evolution

Abstract

Many spliceosomal introns exist in the eukaryotic nuclear genome. Despite much research, the evolution of spliceosomal introns remains poorly understood. In this paper, we tried to gain insights into intron evolution from a novel perspective by comparing the gene structures of cytoplasmic ribosomal proteins (CRPs) and mitochondrial ribosomal proteins (MRPs), which are held to be of archaeal and bacterial origin, respectively. We analyzed 25 homologous pairs of CRP and MRP genes that together had a total of 527 intron positions. We found that all 12 of the intron positions shared by CRP and MRP genes resulted from parallel intron gains and none could be considered to be ''conserved,'' i.e., descendants of the same ancestor. This was supported further by the high frequency of proto-splice sites at these shared positions; proto-splice sites are proposed to be sites for intron insertion. Although we could not definitively disprove that spliceosomal introns were already present in the last universal common ancestor, our results lend more support to the idea that introns were gained late. At least, our results show that MRP genes were intronless at the time of endosymbiosis. The parallel intron gains between CRP and MRP genes accounted for 2.3% of total intron positions, which should provide a reliable estimate for future inferences of intron evolution.

Characterization of intron loss events in mammals

“…Roy and Hartl (2006) studied two relatively closely related Plasmodium species and found a very slow rate of intron loss and possibly no gain during ∼100 Myr of evolution. On the other hand, these results contrast with estimates from fungi (Nielsen et al 2004) and more distantly related eukaryotic clades (Fedorov et al 2002;Rogozin et al 2003;Babenko et al 2004;Roy and Gilbert 2005c;Yoshihama et al 2006), which suggest prevalence of intron gain over intron loss over periods >200 Myr.…”

“…However, ours and other studies in closely related species show a pattern of recurrent intron loss, particularly in highly expressed housekeeping genes that are most likely to recombine with their reverse transcribed cDNA. Because of their high degree of conservation at both sequence and functional levels, such genes are the ones most often used in gene structure comparisons (Rogozin et al 2003;Yoshihama et al 2006). The process of loss is likely to be much more accelerated in organisms with high reproductive rates and large population sizes where selection for reduced transcript length, rather than genetic drift, will lead to fixation of losses in populations.…”

“…It is also likely to be rapid in species with short introns, where recombination with intronless substrates is more efficient. In the presence of recurrent parallel loss, studies using parsimony methods and large evolutionary distances (Rogozin et al 2003;Coghlan and Wolfe 2004;Yoshihama et al 2006) will certainly underestimate the rate of loss and overestimate the rate of intron gains. Even maximum likelihood approaches (Nguyen et al 2005;Roy and Gilbert 2005a;Csuros 2006) are not fully immune to this error and will overestimate the gain rate particularly if they fail to account for the rate variation among sites (Yang 1996), which we have shown to occur in the case of intron loss.…”

Origin of Spliceosomal Introns and Alternative Splicing

“…3). This general strategy can be modified to account for the possibility that general preferences in intron insertion (e.g., into protosplice sites) and/or intron phase biases (reviewed in Rogozin et al 2012) could lead to independent intron insertions occurring at homologous positions in different lineages (Sverdlov et al 2005;Yoshihama et al 2006). Avariety of studies have shown that genes from intron-rich species from any major eukaryotic supergroup share a significant number of intron positions with other groups (Fedorov et al 2002;Rogozin et al 2003;Csurös et al 2008Csurös et al , 2011.…”

Screening and cloning for proteins transactivated by the PS1TP5 protein of hepatitis B virus: A suppression subtractive hybridization study

“…Ribosomal protein is a group of organella involving in cell structure and cell cycle, and possess the important ability to control cell growth, differentiation and adherence. The ribosomal protein is certainly related to cell energy or substance metabolism, and has critical physiological roles in nutrient transport [31] . HBV PS1TP5 protein also interacts with Homo sapiens inositol monophosphatase 2 (IMPA2), Homo sapiens solute carrier family 7 member 5 (SLC7A5), Homo sapiens cytochrome c oxidase subunit 8A, Homo sapiens enolase 1, Homo sapiens H3 histone family 3B, Human cytoskeletal gamma-actin gene, Homo sapiens eukaryotic translation elongation factor 1, Homo sapiens epoxide hydrolase 1, Homo sapiens dehydrogenase 1, Homo sapiens signal sequence receptor-β, Homo sapiens β5-microtubulin and Homo sapiens pyruvate dehydrogenase.…”